Differential Survival between Visual Environments Supports a Role of Divergent Sensory Drive in Cichlid Fish Speciation

Maan, Martine E.; Seehausen, Ole; Groothuis, Ton G. G.

doi:10.1086/689605

Cited by 38 publications

(39 citation statements)

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“…We further show that hybridisation-derived variants are enriched in genes related to vision, pathogen defence and non-coding and ribosomal RNA function. The former two categories have previously been implicated to play a role in speciation and adaptive radiation in cichlids or other fishes (Carleton et al 2005;Malmstrøm et al 2016;Maan et al 2017;Meier et al 2017;Malinsky et al 2018) . In particular, Meier et al (2017) have shown that in the LVRS divergent parental haplotypes of a short-wavelength opsin gene differentiate clear shallow water algivores from deep turbid water detritivores.…”

Section: Discussionmentioning

confidence: 99%

“…5). Both genes related to vision and to pathogen defence have previously been suggested to play a role in speciation (Carleton et al 2005;Malmstrøm et al 2016;Egger et al 2017;Maan et al 2017;Meier et al 2017;Malinsky et al 2018) . Consistent with the results above, we find that even genes in these categories do not show long hybridisation-derived haplotypes, that is, most fixed differences between Ruaha Blue and Victoria in these regions are not variable in Malawi .…”

Section: Hybridisation-derived Variants Are Enriched In Vision-and Immentioning

confidence: 99%

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Ancestral hybridisation facilitated species diversification in the Lake Malawi cichlid fish adaptive radiation

Svardal

Quah

Malinsky

et al. 2019

Preprint

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The adaptive radiation of cichlid fishes in East Afrian Lake Malawi encompasses over 500 species that are believed to have evolved within the last 800 thousand years from a common founder population. It has been proposed that hybridisation between ancestral lineages can provide the genetic raw material to fuel such exceptionally high diversification rates, and evidence for this has recently been presented for the Lake Victoria Region cichlid superflock.Here we report that Lake Malawi cichlid genomes also show evidence of hybridisation between two lineages that split 3-4 million years ago, today represented by Lake Victoria cichlids and the riverine Astatotilapia sp. 'ruaha blue'. The two ancestries in Malawi cichlid genomes are present in large blocks of several kilobases, but there is little variation in this pattern between Malawi cichlid species, suggesting that the large-scale mosaic structure of the genomes was largely established prior to the radiation. Nevertheless, tens of thousands of polymorphic variants apparently derived from the hybridisation are interspersed in the genomes. These loci show a striking excess of differentiation across ecological subgroups in the Lake Malawi cichlid assemblage, and parental alleles sort differentially into benthic and pelagic Malawi cichlid lineages, consistent with strong differential selection on these loci during species divergence. Furthermore, these loci are enriched for genes involved in immune response and vision, including opsin genes previously identified as important for speciation. Our results reinforce the role of ancestral hybridisation in explosive diversification by demonstrating its significance in one of the largest recent vertebrate adaptive radiations.Recent advances in genome sequencing have provided empirical evidence that ancestral hybridisation can occur prior to adaptive radiation (Barrier et al. 1999) and can generate phenotypic novelty (Stryjewski and Sorenson 2017) . A group of species that has received considerable attention with

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Section: Discussionmentioning

confidence: 99%

Section: Hybridisation-derived Variants Are Enriched In Vision-and Immentioning

confidence: 99%

Ancestral hybridisation facilitated species diversification in the Lake Malawi cichlid fish adaptive radiation

Svardal

Quah

Malinsky

et al. 2019

Preprint

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“…Also in contrast to prior work (Dijkstra, Zee, & Groothuis, ; Haesler & Seehausen, ; Seehausen & van Alphen, ; van der Sluijs et al, ), we limited the opportunity for maternal imprinting (Verzijden & ten Cate, ; Verzijden, Korthof, & Cate, ) by removing fish from brooding females at 5 – 6 days post‐fertilization, possibly reducing preference strength. Finally, we are now aware of light‐induced survival differences in our laboratory population: when reared in “unnatural” light conditions, while all other parameters are kept the same, both species survive at a lower rate (~40% reduction at 12 months) than their “naturally” reared counterparts (Maan et al, ). Nonrandom survival could have generated a population of relatively flexible test females, exhibiting weak species specificity in behaviour including mate choice.…”

Section: Discussionmentioning

confidence: 99%

“…Our manipulated light conditions were created to mimic the natural light environments of the blue and red species at Python Islands, Lake Victoria (described in greater detail in: Maan, Seehausen, & Groothuis, ). Briefly, we used halogen light bulbs filtered with a green light filter (LEE # 243, Andover, UK) in both conditions.…”

Section: Methodsmentioning

confidence: 99%

Testing sensory drive speciation in cichlid fish: Linking light conditions to opsin expression, opsin genotype and female mate preference

Wright

Eijk

Schuart

et al. 2019

J of Evolutionary Biology

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Ecological speciation is facilitated when divergent adaptation has direct effects on selective mating. Divergent sensory adaptation could generate such direct effects, by mediating both ecological performance and mate selection. In aquatic environments, light attenuation creates distinct photic environments, generating divergent selection on visual systems. Consequently, divergent sensory drive has been implicated in the diversification of several fish species. Here, we experimentally test whether divergent visual adaptation explains the divergence of mate preferences in Haplochromine cichlids. Blue and red Pundamilia co‐occur across south‐eastern Lake Victoria. They inhabit different photic conditions and have distinct visual system properties. Previously, we documented that rearing fish under different light conditions influences female preference for blue versus red males. Here, we examine to what extent variation in female mate preference can be explained by variation in visual system properties, testing the causal link between visual perception and preference. We find that our experimental light manipulations influence opsin expression, suggesting a potential role for phenotypic plasticity in optimizing visual performance. However, variation in opsin expression does not explain species differences in female preference. Instead, female preference covaries with allelic variation in the long‐wavelength‐sensitive opsin gene (LWS), when assessed under broad‐spectrum light. Taken together, our study presents evidence for environmental plasticity in opsin expression and confirms the important role of colour perception in shaping female mate preferences in Pundamilia. However, it does not constitute unequivocal evidence for the direct effects of visual adaptation on assortative mating.

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“…'pundamilia-like') and one with red/yellow male coloration (P. nyererei and P. sp. both species survive best in their own natural light condition [13].…”

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confidence: 99%

Visual adaptation and microhabitat choice in Lake Victoria cichlid fish

Mameri

Kammen

Groothuis

et al. 2018

Preprint

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15When different genotypes choose different habitats to better match their phenotypes, adaptive 16 differentiation within a population may be promoted. Mating within those habitats may 17 subsequently contribute to reproductive isolation. In cichlid fish, visual adaptation to alternative 18 visual environments is hypothesised to contribute to speciation. Here, we investigated whether 19 variation in visual sensitivity causes different visual habitat preferences, using two closely related 20 cichlid species that occur at different but overlapping water depths in Lake Victoria and that differ 21 in visual perception (Pundamilia sp.). In addition to species differences, we explored potential 22 effects of visual plasticity, by rearing fish in two different light conditions: broad-spectrum 23 (mimicking shallow water) or red-shifted (mimicking deeper waters). Contrary to expectations, fish 24 did not prefer the light environment that mimicked their typical natural habitat. Instead, we found 2 25 an overall preference for the broad-spectrum environment. We also found a transient influence of 26 the rearing condition, indicating that assessment of microhabitat preference requires repeated testing 27 to control for familiarity effects. Together, our results show that cichlid fish exert visual habitat 28 preference, but do not support straightforward visual habitat matching. 29

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Differential Survival between Visual Environments Supports a Role of Divergent Sensory Drive in Cichlid Fish Speciation

Cited by 38 publications

References 64 publications

Ancestral hybridisation facilitated species diversification in the Lake Malawi cichlid fish adaptive radiation

Ancestral hybridisation facilitated species diversification in the Lake Malawi cichlid fish adaptive radiation

Testing sensory drive speciation in cichlid fish: Linking light conditions to opsin expression, opsin genotype and female mate preference

Visual adaptation and microhabitat choice in Lake Victoria cichlid fish

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